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Conservation Biology of Freshwater and : A Compilation ProjectGeoemydidae of the IUCN/SSC — TortoiseMauremys and Freshwater annamensis Specialist Group 081.1 A.G.J. Rhodin, P.C.H. Pritchard, P.P. van Dijk, R.A. Saumure, K.A. Buhlmann, J.B. Iverson, and R.A. Mittermeier, Eds. Chelonian Research Monographs (ISSN 1088-7105) No. 5, doi:10.3854/crm.5.081.annamensis.v1.2014 © 2014 by Chelonian Research Foundation • Published 12 December 2014

Mauremys annamensis (Siebenrock 1903) – , Annam Pond Turtle, Rùa Trung Bộ

Timothy E.M. McCormack1, Jeffrey E. Dawson2,6, Douglas B. Hendrie3, Michael A. Ewert4,8, John B. Iverson5, Ronnie E. Hatcher2,7, and J. Michael Goode2,8

1Asian Turtle Program, Room 1301, Thanh Cong Tower, 57 Lang Ha Street, Hanoi, [[email protected]]; 2Columbus Zoo and Aquarium, P.O. Box 400, Powell, Ohio 43065 USA; 3Education for Nature – Vietnam, Office 1701, 17F, Building 17T5, Hoang Dao Thuy Street, Hanoi, Vietnam [[email protected]]; 4Department of Biology, Indiana University, Bloomington, Indiana 47405 USA; 5Department of Biology, Earlham College, Richmond, Indiana 47374 USA [[email protected]]; 6Present Address: Saint Louis Zoo, 1 Government Drive, St. Louis, Missouri 63110 USA [[email protected]]; 7Present Address: 721 S. Warren Avenue, Columbus, Ohio 43204 USA [[email protected]]; 8Deceased

Summary. – The Vietnamese Pond Turtle, annamensis ( ), is a medium-sized (carapace length to 285 mm in females, 232 mm in males), highly aquatic turtle known only from the lowland wetlands of central Vietnam. Field records are limited and the natural history of M. annamensis is poorly known, in part due to the difficulty in conducting research within the ’ native range as a result of conflict and political isolation during much of the period since its description. Recent work has delimited the historical distribution and gathered evidence for the historical abundance of M. annamensis, but also indicates that the species has largely been extirpated across its range and is now extremely rare in the wild. Over-collection and habitat loss are the greatest contributors to the species’ decline, while pollution and interspecific hybridization may represent additional threats. Substantial international trade in M. annamensis occurred in the past, and despite national and international protection for the species, surviving populations continue to be threatened by intensive collection efforts. In captivity, the species acclimates well and breeds readily, with females capable of producing several clutches of eggs per year. Current conservation efforts include greater enforcement of trade restrictions, the establishment of a protected habitat area, and planning for future reintroductions from captive stocks. Continued research and conservation measures are required to save this species. Distribution. – Vietnam. Historically ranged across central Vietnam coastal lowlands from the municipality of Da Nang and Quang Nam Province south to Phu Yen Province and west into the low-lying inland areas of Gia Lai and Dak Lak provinces. Synonymy. – annamensis Siebenrock 1903, Cuora (Cyclemys) annamensis, Cuora annamensis, Annamemys annamensis, Mauremys annamensis, Annamemys annamemys (ex errore), Cathaiemys annamensis, Annamemys merkleni Bourret 1940, Annamemys mekleni (ex errore), Clemmys guangxiensis Qin 1992 (partim, ), Mauremys guangxiensis, Ocadia glyphistoma McCord and Iverson 1994 (partim, hybrid). Subspecies. – None. Status. – IUCN 2014 Red List: Critically Endangered (CR A1d+2d, assessed 2000); TFTSG Draft Red List: Critically Endangered (CR, assessed 2011); CITES: Appendix II with zero quota for commercial purpose; Vietnam: Decree No. 32/2006/ND-CP.

Taxonomy. — Mauremys annamensis was first described Hoi An town, Quang Nam Province, Vietnam), about 40 km as Cyclemys annamensis by Siebenrock (1903) based on a NE of Phuoc Son. Presumably, Bourret’s error was partly juvenile specimen obtained by H. Fruhstorfer from “Phuc- due to the fact that Siebenrock’s description was based on Son” (= Phuoc Son District, Quang Nam Province, Vietnam). a single immature individual, while Bourret’s specimens Without reference to Siebenrock’s description, Bourret were adults (Savage 1953). Further, Bourret (1941) stated (1940) named the species Annamemys merkleni from a that Siebenrock’s specimen was lost after deposition, which series of eight specimens collected at or near “Fai-Fo” (= would have prevented examination. However, the holotype 081.2 Conservation Biology of Freshwater Turtles and Tortoises • Chelonian Research Monographs, No. 5

Figure 1. Captive adult female Mauremys annamensis. Photo by Jeffrey E. Dawson.

(NMW 23394) has since been located and is in the Museum of designated a lectotype by Savage (1953), who recognized Natural History of Vienna, Austria (Naturhistorisches Museum that A. merkleni was the adult form of C. annamensis and Wien; Tiedemann and Häupl 1980; Tiedemann et al. 1994). In synonymized the taxa. However, Savage (1953) recommended his later monograph on the turtles of , Bourret that the species be retained in the Annamemys, instead (1941) included accounts for both C. annamensis and A. of being placed in Cyclemys, due to the lack of a transverse merkleni. Bourret presented one of the syntypes of A. merkleni plastral hinge in the adult specimens. Subsequently, to the Natural History Museum of Stanford University Annamemys has been synonymized with the genus (Leviton 1953); this specimen (now in the collection of Mauremys (McDowell 1964; Iverson and McCord 1994). the California Academy of Sciences; CAS-SU 9142) was Mauremys guangxiensis, first described as Clemmys guangxiensis by Qin (1992 [1991]), was recently added to the synonymy of M. annamensis (as partim, hybrid) based on the molecular work of Hu et al. (2013); however, the exact relationship of M. guangxiensis to M. annamensis and other taxa is still unresolved and additional research needs to be undertaken (Turtle Working Group 2014). Mauremys annamensis is closely related to M. mutica; excluding studies containing invalid hybrid species (e.g.,

Figure 2. Captive adult female Mauremys annamensis. Photo by Figure 3. Captive adult female Mauremys annamensis. Photo by Jeffrey E. Dawson. Jeffrey E. Dawson. Geoemydidae — Mauremys annamensis 081.3

Figure 4. Historic distribution of Mauremys annamensis in central Vietnam in southeast Asia. Purple lines = boundaries delimiting major watersheds (level 3 hydrologic unit compartments – HUCs); red dots = museum and literature occurrence records of native populations based on Iverson (1992) plus more recent and authors’ data; green shading = projected native historic distribution based on GIS-defined HUCs constructed around verified localities and then adding HUCs that connect known point localities in the same watershed or physiographic region, and similar habitats and elevations as verified HUCs (Buhlmann et al. 2009; TTWG 2014), and adjusted based on authors’ subsequent data.

Honda et al. 2002b), both morphological (Iverson and M. annamensis from central Vietnam forming another McCord 1994) and molecular phylogenetic (Honda et al. clade with M. ‘mutica’ from northern Vietnam (Feldman 2002a; Barth et al. 2004; Spinks et al. 2004) analyses have and Parham 2004). Based on the low number of nucleotide confirmed that the two taxa are each other’s closest living differences between M. annamensis and Vietnamese M. relatives. However, the exact taxonomic relationship between ‘mutica,’ Feldman and Parham (2004) suggested several M. annamensis and M. mutica is unclear. McDowell (1964) possibilities, including that M. annamensis had recently synonymized M. annamensis with M. mutica based on separated from M. mutica, that historical or ongoing gene their similar morphology, yet later morphometric analyses flow occurred between the two species, or thatM. annamensis (Iverson and McCord 1994; Yasukawa et al. 1996) found might simply represent a geographic phenotypic variant of M. annamensis to be distinctive. M. mutica. Initial molecular studies using mitochondrial DNA Incongruences among nuclear DNA (nuDNA), mtDNA, (mtDNA) found substantial differences between M. and morphology were also found by Fong et al. (2007). annamensis and M. mutica (Barth et al. 2004; Spinks et al. Three distinct clades were recovered from the nuDNA – M. 2004). However, a more comprehensive mtDNA study found annamensis, M. ‘mutica’ from Island, , and M. M. mutica to be paraphyletic with respect to M. annamensis, mutica from mainland eastern China. However, only two with M. mutica from eastern China forming one clade and distinct clades were formed by the mtDNA, with mainland

Figure 6. Captive hatchling Mauremys annamensis at Turtle Figure 5. Captive hatchling Mauremys annamensis. Photo by Conservation Centre, Cuc Phuong National Park, Vietnam. Photo Peter Paul van Dijk. by Timothy McCormack, ATP. 081.4 Conservation Biology of Freshwater Turtles and Tortoises • Chelonian Research Monographs, No. 5

Figure 7. Two sections of Co Ni River in Dien Ban District, Quang Nam Province, central Vietnam. Locally caught specimens of Mauremys annamensis are still observed in local trade and apparently caught in this habitat. Photos by Timothy McCormack, ATP.

Figure 8. Ha Tre Lake, situated on a seasonally flooded island in the Thu Bon River, Quang Nam Province, central Vietnam, a site at which Mauremys annamensis was caught in the wild by an ATP team in 2006. Photos by Timothy McCormack, ATP.

M. mutica being a sister clade to the Hainan Island specimens a full species and consider M. mutica as containing multiple and two subclades of M. annamensis. In both studies, the evolutionarily significant units, based on the characteristic incongruent M. ‘mutica’ specimens (northern Vietnam morphological differences between the two taxa (Iverson and Hainan Island) were readily distinguishable from M. and McCord 1994). annamensis morphologically and closely resembled the Mechanisms of reproductive isolation appear to be mainland eastern M. mutica (Feldman and Parham 2004; weak among geoemydid turtles, including M. annamensis. Fong et al. 2007). Human-mediated hybridization has occurred between M. Unfortunately, a rarity of locality-specific specimens of annamensis and Cuora amboinensis (Fritz and Mendau 2002), M. mutica and M. annamensis has hindered all phylogenetic Cuora trifasciata (Zhou et al. 2008), M. mutica (Uhrig and analyses published to date. Genetic samples have primarily Lee 2006; MAE and JMG, unpublish. data), M. nigricans been obtained from specimens acquired from turtle farms (Ipser 2011), and possibly M. reevesii (Spinks and Shaffer or trade seizures; consequently, the specimens could be of 2007) in captivity. anthropogenic hybrid origins, limiting the ability to draw Hybrids have also occurred between M. annamensis conclusions from these studies (Feldman and Parham 2004; and M. sinensis (Spinks et al. 2004). McCord and Iverson Fong et al. 2007; J. Parham, pers. comm.). As a result, (1994) described “Ocadia glyphistoma” based on specimens taxonomic uncertainties continue to exist. Stuart and Parham reportedly from southern China. This species was later (2007) ascribed the incongruent M. ‘mutica’ specimens from shown to be invalid as the specimens were M. annamensis northern Vietnam and Hainan Island to ‘M. cf. annamensis.’ x M. sinensis hybrids that likely had been acquired from However, most authorities have recommended maintaining wildlife markets (Spinks et al. 2004; Stuart and Parham the current taxonomy until further data are available 2007). In Vietnam, hybrids have been observed in the (Feldman and Parham 2004; Fong et al. 2007). Given wildlife trade, including a male specimen of unknown the potential significance to conservation efforts of any origin purchased from Dong Xuan Market, Hanoi in July premature taxonomic changes, we retain M. annamensis as 1999 by one of the authors (DBH) which is currently Geoemydidae — Mauremys annamensis 081.5 maintained at the Turtle Conservation Centre (TCC) in Cuc plastron is sutured to the carapace and the length of the bridge Phuong National Park, Vietnam. Although these hybrids is 40 to 50% the length of the plastron (Ernst and Barbour may originate through captive breeding on turtle farms 1989). Internally, the bridge is extensively buttressed (Savage (Spinks et al. 2004), there is also evidence to suggest that 1953), with thicker bone than is typical of many semi-aquatic natural hybridization may occur in the wild where the species. distributions of the species overlap; several hybrids seen in All scutes of the bridges, plastron, and undersides of Quang Nam province in 2012 were apparently locally wild the marginals include black blotches on a background of caught (Pham 2012; Blanck and Braun 2013; McCormack yellow-orange, horn, or tan. Generally, the bridges and the 2013; McCormack et al. 2013). undersides of the posterior marginals are darker than the Description. — Mauremys annamensis is a medium- undersides of the nuchal and adjacent marginals. The outer sized turtle; a maximum carapace length (CL) of 170 mm margin of the plastron is light colored, while the center of was reported by Ernst and Barbour (1989), but Iverson the plastron has a large, contiguous light area which runs and McCord (1994) documented a female of 285 mm CL, across at least the pectoral, abdominal, and femoral scutes. as do we. A series of mature captive females measured by At its widest, the light area is a third to half as wide as the the current authors (MAE, JBI, JMG) had measurements plastron. Between the light edges and light center are dark (mean ± SD) of 212 ± 28 mm in straight CL (range 189– patches which coalesce posteriorly on the anal scutes and 285 mm, n = 12), 184 ± 26 mm in plastron length (PL; also often at the anterior of the plastron, forming a dark ring range 155–257, n = 12) and 1717 ± 250 g in mass (range across the plastron. 1302–2126 g, n = 8). Adult males are slightly smaller; The head is of moderate size in proportion to the body the largest male known to the authors (JED and REH) is and is somewhat pointed. The temporal arch is complete and a captive specimen with a CL of 232 mm. Captive males the quadratojugal contacts both the jugal and postorbital. measured by the authors (MAE, JBI, JMG) had a CL of Skin on the back of the head is smooth. The background 187 ± 17 mm (range 163–218 mm, n = 16), PL of 153 ± color of the head is slightly lighter to nearly as dark as the 10 mm (132–176 mm, n = 16), and mass of 1066 ± 352 carapace but with an olive green cast. Three prominent pairs g (range 687–1744 g, n = 13). of pale yellow stripes extend posteriorly from near the tip of The carapace is moderately depressed, twice as wide the nose on each side of the head. The faintest pair passes as high, with three longitudinal keels. The median keel is dorsolaterally over the orbits and ends in the temporal area. best developed, while the dorsolateral keels, which run The lateral and most prominent pair runs from the nostrils across the dorsal surfaces of the pleural scutes, are lower. across the orbit and posteriorly along the neck. The third pair Typically, the color of the carapace is uniformly brown extends from below the nostrils along the dorsal border of the (ranging from chestnut to dark brown), gray, or even nearly jaw, below the tympanum, and onto the neck. An additional black, but rarely, there is slight lightening along the keels to set of stripes begins along the inner border of the lower jaw create three faint stripes. Growth annuli are evident on the and passes across the jugular region and onto the neck. The scutes of young specimens; the scutes are worn smooth in central areas of the chin and the throat sport pale yellow. The older . The first vertebral scute is wider anteriorly alveolar surfaces of the jaws are narrow and unserrated; their than posteriorly; the last vertebral scute is the opposite. external color changes from near-white close to the cutting The remaining vertebral scutes are roughly as broad as edges to light gray distally. long (Ernst and Barbour 1989). Lateral to the dorsolateral The limbs have unremarkable length but are muscular. keels, the slope of the carapace dips substantially, and then The toes are not especially long, but are fully webbed. flares outwardly at the marginals. The marginals also flare Generally, the neck, limbs, and tail are dark to medium anteriorly and posteriorly. Viewed from above, the sides of gray dorsally and become lighter gray ventrally. On the the carapace are slightly rounded, with a slightly crenate, or forelimbs, the antebrachia have many enlarged and a few upturned, marginal aspect. The widest point of the carapace sickle-shaped scales, which may be mottled with gray and is in the middle or slightly to the posterior of the middle. pale tan. The axillary and inguinal pockets are cream colored, The rear of the carapace is unserrated. and occasionally mottled with light gray. Maximum PL is roughly 80 to 95% of maximum CL. Hatchlings (n = 41) from eggs produced by captives and The plastron is unhinged and well-developed, but does not measured by the authors (MAE, REH, JMG) were 37.5 ± completely cover the opening of the shell. The anterior lobe 1.9 mm in CL (range 33.8–40.6 mm), 32.5 mm in PL (range is truncate and slightly upturned at the front; the posterior 28.8–35.4 mm), 31.2 ± 1.6 mm in carapace width (range lobe has a deep anal notch. Ernst and Barbour (1989) gave 27.9–33.9 mm), and 9.12 ± 1.2 g in mass (range 6.5–11.0 g). the typical plastral formula as: abd < pect > fem > an > hum The hatchling carapace is tricarinate; however, the median >< gul, but they also noted that the pectoral, abdominal, ridge so dwarfs the lateral ones that the overall effect is and femoral seams are often nearly identical in length. The essentially unicarinate. Hatchlings are colored similarly to 081.6 Conservation Biology of Freshwater Turtles and Tortoises • Chelonian Research Monographs, No. 5

adults but more vivid, with sharper demarcations between Le and Broad (1995) reported that M. annamensis light and dark. All hatchlings of M. annamensis have was abundant in the wildlife trade in Ca Mau Province at prominent, light supraobital stripes on their heads, and a the extreme southern tip of Vietnam. In 2000, a single M. few also have short, light, midsagittal stripes. annamensis was observed in a Ho Chi Minh City market In addition to being slightly smaller, males differ from (Hendrie 2000a). As recent trade routes of turtles in Vietnam females in having distinctly concave rather than flat or mostly typically move northward (Stuart et al. 2000), these flat plastra. The tails of males are appreciably broader at observations suggested that the distribution of M. annamensis the base and more stoutly tapered than those of females, might extend into the Mekong Delta. However, Jenkins but are at most only slightly longer. The cloacal opening is (1995) proposed that the records of Le and Broad (1995) also more distally located along the tails of males. As with were based on misidentified specimens, a view supported by other Mauremys species, hatchlings have long tapering tails. Stuart (2004), who found no evidence of M. annamensis in Iverson and McCord (1994) discussed morphological southern Vietnam. Three species in southern Vietnam (Cuora differences between members of the genus Mauremys. amboinensis, subtrijuga, and juvenile Features which distinguish M. annamensis from M. mutica annandalii) superficially resembleM. annamensis (Hendrie are: 1) a set of head stripes that pass from the snout to above et al. 2011) and frequently appear in trade (Hendrie 2000b). the orbit (not present in M. mutica); 2) a larger maximum size The Ca Pass Mountains along the border of Phu Yen and (at least 285 mm versus 188 mm maximum CL, respectively); Khanh Hoa provinces likely serve as a southern limit for 3) retention of a moderately tricarinate carapace in adult the distribution of M. annamensis. Furthermore, the coastal specimens (smooth to weakly tricarinate in most M. mutica); lowlands near and south of Nha Trang in Khanh Hoa Province 4) female-dominated sexual size dimorphism (either male- have a semi-arid climate (Sterling et al. 2006), which may dominated or lacking in most M. mutica populations); 5) a present an additional barrier to M. annamensis. wider carapace and longer bridge; 6) narrower and longer The range of Mauremys mutica does not appear to overlap gular scutes; 7) a shorter seam between the humeral scutes; that of M. annamensis. The northernmost field-collected and 8) a longer interpectoral seam. specimens of M. annamensis have been reported from Distribution. — The range of M. annamensis appears Quang Nam Province and the city of Da Nang. Mauremys to be restricted to central Vietnam (Iverson 1992; Nguyen annamensis was not present in any shipments of turtles et al. 2009, McCormack 2013). Most published historical from northern Vietnam to Germany in the mid-20th century records originate from Quang Nam Province (Siebenrock (Petzold 1963). During a visit to northern Vietnam, Petzold 1903; Bourret 1940, 1941). The species has also been (1965) failed to locate any individuals of M. annamensis in reported from the centrally-controlled municipality of Da the wild and found only a single specimen of the species in Nang (Dawson et al. 2013) and the provinces of Quang the museum collection at the University of Hanoi. Although Ngai (Turtle Ecology and Conservation Project 2002), Petzold did not state the origin of this specimen, it seems Binh Dinh (Le et al. 2004), and Gia Lai (Parham et al. reasonable to assume that it was collected in central Vietnam 2006). Since 2006, interviews of local people within 11 during colonial times. In contrast, M. mutica has only been provinces that are believed to encompass the species’ range verified in Vietnam from northern locations (Bourret 1941; have been conducted by the Asian Turtle Program (ATP) Tien 1957; Petzold 1963, 1965 [as “Clemmys nigricans”]; of Cleveland Metroparks Zoo. These surveys confirmed Iverson 1992). The sole record of M. mutica in central the historical presence of M. annamensis in the previously Vietnam was in error (see above). listed locations and uncovered other potential sites in Phu The southernmost documented locality for M. mutica (= Yen and Dak Lak Provinces (McCormack et al. 2007; Annamemys grochovskiae) is in Quang Tri Province (Tien McCormack 2013). 1957). However, anecdotal evidence exists for the historical A specimen of M. annamensis in the Toulouse Museum occurrence of M. mutica just to the south of Quang Tri in was collected by Bourret in the early 20th century with Thua Thien Hue Province. Descriptions provided by local the locality data of Nha Trang (Khanh Hoa Province) and people match this species; these reports likely represent apparently mislabeled as M. mutica (R. Bour, pers. comm.). the historical southern limit of M. mutica in Vietnam However, interview surveys in 2011 and 2012 failed to find (McCormack 2013). The Hai Van Pass of the Truong Son any information regarding wild M. annamensis in Khanh Range (Annamite Mountains) appears to be a natural physical Hoa Province (McCormack 2013). While it is possible boundary between the southern extent of M. mutica and the that the species once inhabited the area and has since been northern limit of M. annamensis (Le et al. 2004). extirpated, it is more likely that the specimen originated in In recent years, the range of M. annamensis has another location and was then transported to Nha Trang, contracted significantly. Throughout much of its range, local which was an important regional town situated on the major people consider it to be extremely rare (McCormack 2013). trade route in Vietnam. Currently, only isolated individuals and a few fragmented Geoemydidae — Mauremys annamensis 081.7 relic populations are thought to remain in the wild. Recent dry season by probing the litter at the base of bamboo interviews of turtle collectors and traders within a few stands with bamboo poles tipped with metal, listening for a scattered districts in the provinces of Binh Dinh, Phu Yen, distinctive sound when the carapace was hit (Asian Turtle Quang Ngai (McCormack 2013), and Quang Nam (Duc Program, unpubl. data). In the wet season, flood events are and Nguyen 2001; McCormack et al. 2007; McCormack common, and M. annamensis likely disperses during these 2013) have indicated that people in these areas continue seasonal floods. Local people recall the capture of turtles to be familiar with M. annamensis. In 2006, a single clinging to tree branches in gardens and fields during floods wild specimen was caught during an ATP field survey in in the past (ATP, unpubl. data). Quang Nam Province, roughly 10 km from Hoi An, where No information is available on the natural predators Bourret’s specimens were reportedly obtained in the 1930s of M. annamensis; however, Iverson and McCord (1994) (McCormack et al. 2007). Recent reports from Da Nang and Yasukawa et al. (1996) suggested that the shape and consist only of specimens in trade and restaurants (Le et al. heavy buttressing of the shell of M. annamensis may have 2004; Tran Thi An Huong, pers. comm.). evolved in response to predation pressure by crocodilians. At Habitat and Ecology. — Mauremys annamensis appears a number of sites throughout its range, M. annamensis has to be restricted to low elevations, less than 200 m above likely occurred sympatrically with the Siamese Crocodile sea level (McCormack 2013). This is most apparent in the (Crocodylus siamensis), as is evident in Song Hinh district, mountainous provinces of Gai Lai and Dak Lak, where M. Phu Yen province, where remnant crocodilian populations annamensis has been reported by local people only from occur (Nguyen et al. 2005; Simpson and Bezuijen 2010). low elevations in the eastern regions of these provinces, Mauremys annamensis is likely a generalist feeder, and appears to have historically been absent from higher but the natural diet is unknown. In captivity, the species elevations to the west (McCormack 2013). Turtle traders in is omnivorous, but demonstrates a strong preference for Quang Nam Province associate M. annamensis with “streams, carnivory. ponds, and swamps” in valleys (Duc and Nguyen 2001). The reproductive behavior of M. annamensis is known In central Vietnam, hundreds of streams carry water only from captive observations. During courtship, males down from the Truong Son Range and across the lowlands will often bite and hold females by the nape of the neck, before draining into the South China or East Sea (Sterling clapping their plastrons against the carapaces of the females et al. 2006). Originally, M. annamensis likely inhabited the before attempting intromission. A receptive female quickly lowland freshwater marshes and slow-moving waterways assumes a submissive position with her neck, limbs, and tail connected to these streams. Floore et al. (1971) characterized fully extended and limp. If the female is unwilling, however, these wetlands as having sandy, clay soil and abundant a violent struggle may ensue (Gurley 2003; JED and REH, floating and submerged vegetation. The margins of the pers. obs.). These behaviors are very similar to the copulatory marshes supported ferns, sedges, and grasses, with the behaviors of M. mutica (Yasukawa et al. 1996) and unlike surrounding upland habitat consisting of bamboo stands, those described for M. japonica (Yasukawa et al. 2008). leading to xeric herbs and shrubs in higher areas (Floore Under semi-natural conditions at the Turtle Conservation et al. 1971). Most of this lowland habitat has now been Centre (TCC) in Cuc Phuong National Park, Vietnam, nests converted to agriculture and urban areas (Thuy et al. 2000) of M. annamensis have been discovered in May and June and M. annamensis currently appears restricted to ponds and (McCormack and Bui 2005). Captives in Indiana and Ohio fragmented wetlands scattered among rice fields and along in the United States have been found gravid from the last riparian corridors (McCormack 2013). week of March to the first week of August (MAE and JMG, Mauremys sinensis appears to occur sympatrically with unpubl. data). The shells of eggs are rigid and brittle. Eggs M. annamensis. Both species have been reported from the obtained under captive conditions in the United States and same wetland and lake complex during Asian Turtle Program measured by the authors (MAE, REH, JMG) averaged 45.3 (ATP) surveys in Quang Ngai province (McCormack 2013; ± 3.7 mm in length, 23.6 ± 1.1 mm in width, and 15.5 ± 2.5 McCormack et al. 2013). g in mass (n = 293). Females (n = 8) laid 1–4 (median 2) Little is known about the biology of M. annamensis in the clutches of eggs per year, with 5.5 ± 1.6 eggs per clutch (n wild. Most observations of behavior, diet, and reproduction = 53) and a maximum of 17 eggs per female in a season. are from captivity. The lowlands of central Vietnam Relative clutch mass (clutch mass/spent female mass) varied experience a monsoon climate with distinct dry (January from 0.033 to 0.104 (MAE and JMG, unpubl. data). through September) and wet (October through December) The rate of embryonic development is determined seasons (Sterling et al. 2006; Yen et al. 2011). During the by temperature, with incubation length ranging between dry season, M. annamensis may estivate on land, particularly 114–131 days at 25°C (n = 11), 93–104 days at 27°C (n = within bamboo stands. Formerly, when the species was more 3), and 80–83 days at 30°C (n = 8) (MAE, unpubl. data). abundant, hunters would locate M. annamensis during the Sex differentiation is controlled by temperature during 081.8 Conservation Biology of Freshwater Turtles and Tortoises • Chelonian Research Monographs, No. 5

embryonic development (temperature-dependent sex 1980s; in some areas, the species was even considered a pest, determination, TSD), with M. annamensis, along with other as large individuals would flatten trails through rice crops or Mauremys studied thus far (Ewert and Nelson 1991; Du et walk into houses. Some locals report collecting rice sacks al. 2007; Du et al. 2010; Okada et al. 2010), following TSD full of turtles (likely including both M. annamensis and M. Pattern Ia, in which males are produced at lower constant sinensis in areas where these species occur sympatrically) incubation temperatures and females at higher constant nightly during the 1980s (ATP, unpubl. data). temperatures (Ewert et al. 2004). The pivotal temperature, Since that time, only a few specimens have been the constant temperature which produces an equal sex ratio documented outside of captivity (Parham et al. 2006; (1:1), has been estimated to be 28.9°C for M. annamensis McCormack et al. 2007). One wild specimen was caught (Ewert et al. 2004). in Quang Nam Province during a field survey in 2006 Information on growth, maturation, and longevity of (McCormack et al. 2007), but since 2009, additional trapping M. annamensis is scarce and only available from captive at other locations with apparently suitable habitat has failed individuals. A series of females (n = 16), bred in the United to locate other specimens (McCormack 2013). Today, M. States and continuously provided with adequate growing annamensis appears to be extremely rare in the wild and is conditions, reached a mean CL of 157 ± 8 mm (range apparently extant only at low densities in a few remaining 145–174 mm), PL of 134 ± 12 mm (range 117–159 mm), isolated populations. and mass of 676 ± 104 g (range 497–834 g) at 4.75 yrs of age Threats to Survival. — The greatest threat to the (Columbus Zoo and Aquarium, unpubl. data). In captivity, survival of M. annamensis is the so-called Asian Turtle females mature when they reach approximately 180 mm CL Crisis (Hendrie 2000b) – the expansive international trade at roughly 5–7 years old (MAE, JED, REH, JMG, unpubl. in Asian chelonians for food, traditional medicine, and pets data). The longevity record for this species in captivity is (van Dijk et al. 2000). Most M. annamensis that entered approximately 46 years for an individual currently living the international trade were destined for consumption in at the Columbus Zoo (Dawson et al. 2013); several other China. Local people in Vietnam state that collection of this individuals in the same collection, received as young adults species for trade to China began in the 1980s and increased in the early 1990s, are still alive in 2014 and reproductively rapidly (ATP, unpubl. data). Subsequently, the species has active at approximately 25–30 yrs of age. been widely observed in the markets of southern mainland Population Status. — Bourret (1941) described M. China (Wildlife Conservation Society – China Program annamensis as being abundant in the ponds and streams within and China Endangered Species of Wild Fauna and Flora the area surrounding Hoi An. However, no quantitative data Import and Export Administrative Office 2000; Artner and exist to support this statement. Due to regional warfare and Hofer 2001; Lee et al. 2004), Hainan Island (de Bruin and political isolation that subsequently ensued, almost nothing Artner 1999), and Hong Kong (Cheung and Dudgeon 2006). is known about the status of M. annamensis during the next Beginning around 1990, M. annamensis also appeared in several decades; only one individual from this time period the pet trade in Europe, , and the United States is known, collected in 1966 near Da Nang by a U.S. Navy (Altherr and Freyer 2000; China and Germany 2002; JMG corpsman (Dawson et al. 2013). However, interviews of local and REH, pers. obs.). people indicate that M. annamensis was locally common in In Vietnam, M. annamensis was regularly found in trade many areas throughout its range during the 1970s and early seizures headed toward China prior to 1998, but observations in the trade declined afterward (Hendrie 2000b). This decline likely resulted from a reduction in the number of turtles in the wild, which made collection more difficult (Hendrie 2000b) and increased the economic value of M. annamensis in the trade, possibly prompting authorities to permanently confiscate fewer animals; instead, turtles may have been briefly impounded, then sold back into the trade using regulatory loopholes without being reported (ATP, unpubl. data). In addition to international trade, local consumption for food and purported medicinal benefits has been documented (McCormack et al. 2013). Small numbers of M. annamensis Figure 9. Wild-caught subadult female Mauremys annamensis continue to be found in the possession of people in central from Dien Ban District, Quang Nam Province, Vietnam, 2006. This appeared to have injuries from a fire; bamboo stands Vietnam; at a single location in Quang Ngai province, 13 are sometimes cleared using fire and the turtles are reported to turtles were seen in local households between May 2008 estivate during the dry season in the base of bamboo. Photo by Timothy McCormack, ATP. and July 2013 (McCormack 2013; McCormack et al. Geoemydidae — Mauremys annamensis 081.9

2013). Currently, the economic incentive for local people used to defoliate forests and destroy crops (Stellman et al. to collect turtles continues to exist. Whereas M. annamensis 2003). Dioxin, a potent and persistent toxin, was an impurity previously had a relatively modest value in the trade (Duc in some of these chemical defoliants (Schecter et al. 2006). and Nguyen 2001), individuals now command a much Soil contamination and the subsequent bioaccumulation of higher price (McCormack et al. 2013). In particular, the dioxin in the tissues of organisms have occurred at some cost appears to have risen dramatically since 2011 (ATP, former sites of herbicide handling and application, including unpubl. data). in central Vietnam (Dwernychuk et al. 2002). Due to the increased economic value of M. annamensis, Following the end of the war, as urbanization within farming operations targeting this species have now begun the range of M. annamensis has increased, additional (McCormack 2013; McCormack et al. 2013). However, pollutants (such as untreated sewage and heavy metals) have rather than relieve the pressure on M. annamensis in the been discharged from residential areas and industries into wild, these farms have further increased demand for the the waterways and soil (Thuy et al. 2000; Danang Urban species through the need for breeding stock. As a result, Environment Company 2003), while pesticide and herbicide most specimens in the trade are now reportedly destined usage has also increased. In Quang Ngai Province, an oil for farms in Vietnam and China (ATP, unpubl. data). While refinery and industrial zone has been built in a coastal area near some breeding is reported by farmers, turtles caught from one of the last known remnant M. annamensis populations the wild may also be laundered through farms and resold (ATP, unpubl. data). as being captive-bred (McCormack 2013). Farmers have The possible effects of environmental contaminants also established ‘pyramid schemes’ where existing farms on remaining M. annamensis populations in the wild are sell hatchlings to new farms, promising high returns on unknown. However, in other turtle species, dioxin and other investments, but providing little information on how to sell toxic chemicals have been implicated in developmental to end consumers (ATP, unpubl. data). Such speculative abnormalities (Bishop et al. 1998) and reproductive impairment farming activities have already had negative impacts on (Shelby-Walker et al. 2009). Bioaccumulated contaminants in other types of wildlife in Vietnam (Wildlife Conservation M. annamensis may also present risks to human consumers, Society 2008; Brooks et al. 2010). as has been shown in other species of turtles utilized for food Another major threat to M. annamensis is habitat and traditional medicine (Green et al. 2010). destruction. The lowlands of central Vietnam have an The rarity of M. annamensis in the wild may hinder extended history of human occupation (Sterling et al. 2006). the remaining mature individuals from finding suitable Despite this long period of settlement and the anthropogenic mates (McCormack et al. 2013), increasing the potential changes to the landscape (such as agricultural conversion) for genetic bottlenecks, genetic drift, and genetic mixing that occurred during this time (Floore et al. 1971), M. through interspecific hybridization. In 2012, seven juvenile annamensis has persisted in the wild until relatively recently turtles, apparent hybrids between M. annamensis and M. (McCormack et al. 2013). However, the loss of habitat to sinensis, were reputedly discovered in the wild by local intensive rice cultivation and urban areas has increased people at a site in Quang Ngai Province (Blanck and Braun dramatically as the human population of Vietnam has grown 2013; McCormack 2013; McCormack et al. 2013). All of tremendously in the 20th century (Sterling et al. 2006). The the turtles were reportedly caught when a small pond was area between Da Nang and Hoi An is now a major socio- drained (Pham 2012; Blanck and Braun 2013). economic center of Vietnam (Thuy et al. 2000) and Da Conservation Measures Taken. — Mauremys Nang is currently one of the largest, most highly urbanized, annamensis has been listed by the IUCN Red List of and most densely populated Vietnamese cities (Da Nang as Critically Endangered since 2000 Urban Environment Company 2003; Sterling et al. 2006). (IUCN 2014) and is included among the world’s top 25 Many watercourses in the area have been substantially most endangered tortoises and freshwater turtles (Turtle impacted by channelization, filling of low-lying areas, Conservation Coalition 2011). A proposal to add M. and draining of wetlands (Da Nang Urban Environment annamensis to CITES Appendix II (China and Germany Company 2003). Although M. annamensis could potentially 2002) was accepted in 2002. At the sixteenth meeting of the still inhabit some of these modified habitats (e.g., flooded Conference of the Parties in 2013, the Socialist Republic rice fields or urban canals), turtles in these areas have a of Vietnam (2012) proposed transferring the species from greater chance of human contact, leading to an increased Appendix II to Appendix I. However, an alternate proposal potential for collection. which retained M. annamensis on Appendix II but included Chemical pollution may pose additional problems for a zero export quota for commercial purposes (China and M. annamensis. In the 1960s and early 1970s, the entire United States 2012) was approved instead. distribution of M. annamensis was located within a war Within Vietnam, M. annamensis is listed as Critically zone. During this conflict, large quantities of herbicides were Endangered in the Vietnam Red Data Book (Tran et al. 2007). 081.10 Conservation Biology of Freshwater Turtles and Tortoises • Chelonian Research Monographs, No. 5

The species is partially protected by a listing in Group 2B FPD, and the local People’s Committee have started working (animals with restricted exploitation and use for commercial to establish a Species Habitat Conservation Area (SHCA), purposes) of Decree No. 32/2006/ND-CP (Socialist Republic a proposed area of roughly 100 ha of protected habitat. of Vietnam 2006). However, in a draft revision of this law, Formation of the protected area is still being negotiated, as M. annamensis is recommended for up-listing to Group fragmentation of the habitat and usage of the area by local 1B (animals prohibited from exploitation for economic households makes creation of a protected area challenging purposes). (McCormack et al. 2013). Enforcement of trade regulations has been inconsistent In addition to protecting vital habitat for the species, and problematic in the past (Hendrie 2000a, 2000b), but has the proposed creation of a Turtle Assurance Colony (TAC) shown recent improvement (McCormack 2013). Between at the SHCA would allow for the housing and breeding 2000 and 2009, no confiscations of M. annamensis were of a captive group of M. annamensis, with the goal of turned over to conservation organizations. Since then, M. producing offspring for future release into the SHCA annamensis has been seized by officials in Quang Ngai (McCormack et al. 2013). Furthermore, the TAC would Province (Education for Nature – Vietnam 2009) and Khanh permit the quarantine of captive-bred animals transferred Hoa Province (Hoang and Wahl 2013) and transferred to a to Vietnam from international captive assurance colonies. captive assurance population for conservation purposes. Already, M. annamensis have been relocated from the These confiscations can be partly attributed to increased Kadoorie Farm and Botanic Garden in Hong Kong local awareness about the status and conservation needs of (Anonymous 2006), the Rotterdam Zoo in the Netherlands, M. annamensis in central Vietnam. and the Münster Zoo and a private breeder in Germany Since 2009, the Asian Turtle Program (ATP) of (Education for Nature – Vietnam 2013) to the TCC in Cleveland Metroparks Zoo has conducted school programs, Cuc Phuong National Park. These transfers have greatly community activities, and professional training courses boosted the captive assurance population in Vietnam in (including enforcement training with a focus on and terms of numbers and genetic lineages (Education for freshwater turtles for authorities) throughout the species’ Nature – Vietnam 2013). range (McCormack 2013). Additionally, ex-situ captive Captive Husbandry. — Aspects of the husbandry of assurance colonies of M. annamensis are held in Vietnam at M. annamensis have been previously described by Gurley the Turtle Conservation Centre in Cuc Phuong National Park (2003), Uhrig and Lee (2006), Artner (2007), and Stern (McCormack et al. 2013) and internationally in both Europe (2014). Overall, M. annamensis acclimates well to a range (Raffel and Meier 2013) and the United States (Schaffer of captive conditions. Individuals may be maintained in 2006; Turtle Conservation Coalition 2011). groups provided that care is taken to watch for intraspecific Conservation Measures Proposed. — Mauremys aggression (in particular, extremely active courting males annamensis is not currently known to inhabit any protected may injure or drown other individuals when held together areas in Vietnam (Turtle Conservation Coalition 2011; in close quarters for long periods; Gurley 2003; JED and McCormack et al. 2013). Existing protected areas within REH, pers. obs.). Mauremys annamensis can be successfully the range of M. annamensis include Son Tra Nature Reserve housed with other aquatic turtle species (López et al. 2001; in Da Nang, Phu Ninh Nature Reserve in Quang Nam Uhrig and Lee 2006; Artner 2007; JED and REH, pers. obs.); Province, An Toan Nature Reserve in Binh Dinh Province, however, the frequency with which the species hybridizes A Yun Pa Nature Reserve in Gia Lai Province, Ea So Nature with other Asian geoemydids in captivity suggests that Reserve in Dak Lak Province, and Krong Trai Nature assurance colonies should be maintained in isolation from Reserve and Deo Ca Hon Nha Special Use Forest in Phu related species. Yen Province (Tordoff et al. 2004). Although M. annamensis Outdoor ponds, greenhouses, and indoor enclosures could potentially occur in these protected areas, significant with artificial lighting have all been used successfully. As numbers of turtles are unlikely to be supported as suitable M. annamensis is only a moderately good swimmer, water wetland and pond habitat is in limited availability with deeper than 2 m and steep-sided pools should be avoided. mostly rivers and streams occurring there. An ample land area with both open and sheltered spots In 2010, the ATP, working with the provincial Forest should be provided. Captive specimens tend to remain shy Protection Department (FPD), identified a complex of and secretive. Although M. annamensis is active during both lakes, wetlands, and other habitat that appears suitable for the day and night, there is a trend towards greater nocturnal M. annamensis in Binh Son District, Quang Ngai Province activity (Uhrig and Lee 2006; Artner 2007; JED and REH, (McCormack 2013; McCormack et al. 2013). Mauremys pers. obs.). sinensis is known to occur at the locality and specimens of Captive M. annamensis tolerate a range of environmental M. annamensis are still occasionally encountered in local temperatures, from 40°C in the summer down to 4–8°C in trade surrounding the site (McCormack et al. 2013). ATP, winter (Uhrig and Lee 2006; Artner 2007). Turtles kept Geoemydidae — Mauremys annamensis 081.11 indoors seem to do well in water temperatures between of M. annamensis are held in the private sector in both the 24–27°C. Use of lighting which provides a natural United States and Europe (JED, pers. obs.). photoperiod and ultraviolet radiation in basking areas is Current Research. — An attempt to examine genetic recommended for indoor enclosures. Captive specimens variation within the genus Mauremys using genetic material will accept a wide variety of foods, including earthworms, acquired from historical museum specimens of M. annamensis insects, fish, commercial turtle pellets, aquatic vegetation, through ancient DNA techniques and from a living specimen green leafy vegetables, , and fruit. Individuals housed of known locality is on-going (J. Parham, pers. comm.; B. outdoors have been observed catching and consuming newly Stuart, pers. comm.). Additionally, DNA analysis of captive- metamorphosed frogs (Uhrig and Lee 2006). Artner (2007) bred animals is being undertaken in Vietnam to ensure genetic reported feeding almost exclusively a homemade gelatin suitability before release (McCormack et al. 2013). diet, with good success. Mauremys annamensis reproduces readily under Acknowledgments. — Support was provided by human care. Successful breeding has occurred in China Cleveland Metroparks Zoo (TEMM, DBH), Columbus (Li et al. 2002), Japan (Kawata 2003), the United States Zoo and Aquarium (JED, REH, JMG), Earlham College (Gurley 2003; Uhrig and Lee 2006; MAE, JED, REH, (JBI), Indiana University-Bloomington (MAE), and Saint pers. obs.), Europe (Artner 2007; Raffel and Meier 2013), Louis Zoo (JED). The Critical Ecosystem Partnership and Vietnam (McCormack and Bui 2005). At the TCC Fund, Disney Worldwide Conservation Fund, U.S. Fish in Cuc Phuong National Park (roughly 550 km north of and Wildlife Service, the IUCN Netherlands, and the Turtle the northern distribution limit of M. annamensis), natural Conservation Fund provided support for the conservation incubation of nests laid in outdoor enclosures has been activities of the Asian Turtle Program. We sincerely thank successful (McCormack and Bui 2005). However, artificial Roger Bour, Bui Dan Phong and the Turtle Conservation incubation, with the eggs partially buried in damp substrate Centre (TCC) of Cuc Phuong National Park in Vietnam, (approximately 1:1 mixture of coarse vermiculite to water by Elizabeth Burke, Flora Ihlow, the late Jack McCoy, Craig weight), is typically utilized in captive breeding operations. Nelson, James Parham, and Bryan Stuart for their insights Artner (2007) reported that embryos enter diapause in the and assistance. Thanks to Becky Ellsworth, Lewis Greene, middle of incubation and described cooling eggs at 20–23°C Patty Peters, and Doug Warmolts of the Columbus Zoo and for 3–4 weeks in to increase hatching rate. However, Aquarium for reviewing this manuscript and allowing the use Uhrig and Lee (2006) achieved hatching rates of >85% of previously unpublished data. We would also like to thank over 5 years without utilizing a cooling period. Similarly, the Forest Protection Departments and Provincial Peoples the current authors (MAE, JED, REH, pers. obs.) have used Committees in Da Nang, Quang Nam, Quang Ngai, Binh constant incubation temperatures and found no evidence of Dinh, Phu Yen, Khanh Hoa, Gia Lai and Dak Lak provinces post-ovipositional arrest in embryos of M. annamensis. The for support of research and conservation activities in central reason for this discrepancy between incubation methods is Vietnam. not readily apparent. Long-term captive and captive-bred M. annamensis are LITERATURE CITED hardy and the incidence of disease in these individuals is Altherr, S. and Freyer, D. 2000. The decline of Asian turtles: food low. As with other captive , over-feeding can result markets, and pet trade drive Asia’s freshwater in morbid obesity. Occasional episodes of reluctance to nest, turtles and tortoises to . Munich, Germany: Pro Wildlife, leading to dystocia and rapid overcalcification of the egg shell, 23 pp. may occur, but females typically respond well to injections Anonymous. 2006. Endemic Vietnamese Pond Turtles come of the hormone oxytocin, as described by Ewert and Legler home. Press release of the Asian Turtle Program. http:// www.asianturtleprogram.org/pages/map_project/ (1978). Fungal infections can occur in situations when water Mauremys_come_home_May06/Endemic-Vietnamese-pond- parameters are unsuitable or basking areas are insufficient turtles-return-11May06.pdf (Uhrig and Lee 2006; JED, REH, TEMM, pers. obs.). Artner, H. 2007. Chilling the eggs during incubation as the key to A studbook is maintained for specimens of M. annamensis successful breeding of the Annam Leaf turtle Mauremys annamensis held in North American zoological institutions (Stern 2014), (Siebenrock, 1903). 14(1):19–32. Artner, H. and Hofer, A. 2001. Observations in the Qing Ping free but interest in the management of this species within zoos has market, Guangzhou, China, November 2000. Turtle and Tortoise traditionally been low (Association of Zoos and Aquariums Newsletter 3:14. Chelonian Advisory Group 2006). As of August 2013, the Association of Zoos and Aquariums Chelonian Advisory Group. Zoological Information Management System (International [Quinn, H. (Ed.)]. 2006. AZA regional collection plan. Silver Spring, Species Information System 2013) reported 65 individuals MD: Association of Zoos and Aquariums, 102 pp. Barth, D., Bernhard, D. Fritzsch, G., and Fritz, U. 2004. The housed in 11 North American zoos and aquariums and 120 freshwater turtle genus Mauremys (Testudines, Geoemydidae) - individuals in 16 European zoos. A much larger number a textbook example of an east-west disjunction or a taxonomic 081.12 Conservation Biology of Freshwater Turtles and Tortoises • Chelonian Research Monographs, No. 5

misconcept? Zoologica Scripta 33(3):213–221. report to Cuc Phuong Turtle Conservation and Ecology Project, 15 pp. Bishop, C.A., Ng, P., Pettit, K.E., Kennedy, S.W., Stegeman, Dwernychuk, L.W., Hoang, D.C., Hatfield, C.T., Boivin, T.G., Tran, J.J., Norstrom, R.J., and Brooks, R.J. 1998. Environmental M.H., Phung, T.D., and Nguyen, D.T. 2002. Dioxin reservoirs in contamination and developmental abnormalities in eggs and southern Viet Nam—a legacy of Agent Orange. Chemosphere hatchlings of the ( serpentina 47(2):117–137. serpentina) from the Great Lakes-St Lawrence River basin (1989- Education for Nature – Vietnam. 2009. Critically endangered turtles 1991). Environmental Pollution 101(1):143–156. rescued from trade. ENV News Brief E299. Blanck, T. and Braun, S. 2013. Zentral-Vietnam: Ostasiatischen Education for Nature – Vietnam. 2013. Coming home: opportunities “Bachschildkröten” und Hybriden auf der Spur. Marginata 38:18–30. for conservation of the endemic Vietnamese Pond Turtle. Press Bourret, R. 1940 [1939]. Notes herpétologiques sur l’Indochine release, http://envietnam.org/images/News_Resources/Press_ Française, XVIII. Reptiles et batraciens reçus au Laboratoire Releases/19%20aug%202013.pdf des Science Naturelles de l’Université au cours de l’année 1939. Ernst, C.H. and Barbour, R.W. 1989. Turtles of the World. Washington, Descriptions de quatre espècies et d’une variété nouvelles. Annexe DC: Smithsonian Institution Press, 313 pp. au Bulletin Générale de l’Instruction Publique, Hanoi 1939(4):5–39. Ewert, M.A. and Legler, J.M. 1978. Hormonal induction of oviposition Bourret, R. 1941. Les tortues de l’Indochine. Institut Océanographique in turtles. Herpetologica 34(3):314–318. Indochine 38:1–235. Ewert, M.A. and Nelson, C.E. 1991. Sex determination in turtles: Brooks, E.G.E., Roberton, S.I., and Bell, D.J. 2010. The conservation diverse patterns and some possible adaptive values. Copeia impact of commercial wildlife farming of porcupines in Vietnam. 1991(1):50–69. Biological Conservation 143(11):2808–2814. Ewert, M.A., Etchberger, C.R., and Nelson, C.E. 2004. Turtle Buhlmann, K.A., Akre, T.S.B., Iverson, J.B., Karapatakis, D., Mit- sex-determining modes and TSD patterns, and some TSD pattern termeier, R.A., Georges, A., Rhodin, A.G.J., van Dijk, P.P., and correlates. In: Valenzuela, N. and Lance, V.A. (Eds.). Temperature Gibbons, J.W. 2009. A global analysis of tortoise and freshwater Dependent Sex Determination in Vertebrates. Washington, DC: turtle distributions with identification of priority conservation areas. Smithsonian Institution Press, pp. 21–32. Chelonian Conservation and Biology 8(2):116–149. Feldman, C.R. and Parham, J.F. 2004. Molecular systematics of Cheung, S.M. and Dudgeon, D. 2006. Quantifying the Asian turtle Old World stripe-necked turtles (Testudines: Mauremys). Asiatic crisis: market surveys in southern China, 2000 – 2003. Aquatic Herpetological Research 10:28–37. Conservation: Marine and Freshwater Ecosystems 16(7):751–770. Floore, T.G., Grothaus, R.H., and Miner, W.F. 1971. Seasonal China and Germany. 2002. CITES CoP12, Proposition 21 - Inclusion mosquito fluctuations in Da Nang, South Vietnam, based on three of Annam Pond Turtle Annamemys (Mauremys) annamensis in prevalent species. Mosquito News 31(3):416–421. Appendix II. Geneva, Switzerland: CITES Secretariat, 9 pp. http:// Fong, J.J., Parham, J.F., Shi, H., Stuart, B.L., and Carter, R.L. 2007. www..org/eng/cop/12/prop/E12-P21.pdf. A genetic survey of heavily exploited, endangered turtles: caveats China and United States. 2012. CITES CoP16, Proposition 32 - on the conservation value of trade animals. Animal Conservation Inclusion of the following taxa of the Family Geoemydidae in 10(4):452–460. Appendix II: Cyclemys spp., japonica, G. spengleri, Fritz, U. and Mendau, D. 2002. Ein Gattungsbastard zweier Hardella thurjii, Mauremys japonica, M. nigricans, südostasiatischer Schildkröten: Cuora amboinensis kamaroma trijuga, petersi, bealei, S. quadriocellata and Rummler & Fritz, 1991 x Mauremys annamensis (Siebenrock, Vijayachelys silvatica and adoption of a zero quota on wild specimens 1903). Salamandra 38(3):129–134. for commercial purposes for borneoensis, B. trivittata, Green, A.D., Buhlmann, K.A., Hagen, C., Romanek, C., and Gibbons, Cuora aurocapitata, C. flavomarginata, C. galbinifrons, C. mccordi, J.W. 2010. Mercury contamination in turtles and implications for C. mouhotii, C. pani, C. trifasciata, C. yunnanensis, C. zhoui, human health. Journal of Environmental Health 72(10):14–22. Heosemys annandalii, H. depressa, Mauremys annamensis, and Gurley, R. 2003. Keeping and Breeding Freshwater Turtles. Ada, Orlitia borneensis. Geneva, Switzerland: CITES Secretariat, 25 OK: Living Art Publishing, 297 pp. pp. http://www.cites.org/eng/cop/16/prop/E-CoP16-Prop-32.pdf. Hendrie, D.B. 2000a. Compiled notes on the wildlife trade in Vietnam, Danang Urban Environment Company. 2003. Vietnam three cities January – May 2000. Cuc Phuong Conservation Project Report to sanitation project: Danang sub-project, Vol. 10: environmental TRAFFIC Southeast Asia, 9 pp. impact assessment. Report to the World Bank. http://www-wds. Hendrie, D.B. 2000b. Status and conservation of tortoises and worldbank.org/servlet/WDSContentServer/WDSP/IB/2003/10/10/ freshwater turtles in Vietnam. In: van Dijk, P.P., Stuart, B.L., and 000094946_0309300404042/Rendered/PDF/multi0page.pdf. Rhodin, A.G.J. (Eds). Asian Turtle Trade. Chelonian Research Dawson, J.E., Hatcher, R.E., and Calloway-Burke, G.E. 2013. Monographs 2. Lunenburg, MA: Chelonian Research Foundation, Mauremys annamensis: locality and longevity. Herpetological pp. 63–73. Review 44(1):91–93. Hendrie, D.B., Bui, D.P., McCormack, T., Hoang, V.H., and van de Bruin, R.W.F. and Artner, H.G. 1999. On the turtles of Hainan Island, Dijk, P.P. 2011. [Tortoise and Freshwater Turtle Identification southern China. Chelonian Conservation and Biology 3(3):479–486. Resource] (in Vietnamese). Hanoi, Vietnam: Education for Nature Du, W.-G., Hu, L.-J., and Zhu, L.-J. 2007. Effects of incubation – Vietnam, Cuc Phuong Turtle Conservation Centre, and Asian temperature on embryonic development rate, sex ratio and post- Turtle Program, 66 pp. hatching growth in the Chinese three-keeled pond turtle, Chinemys Hoang, V.T. and Wahl, S. 2013. Web monitoring and collaboration reevesii. Aquaculture 272:747–753. with Khanh Hoa officials lead to the rescue of critically Du, W.-G., Wang, L., and Shen, J.-W. 2010. Optimal temperatures endangered Vietnamese Pond Turtles. Press release of the Asian for egg incubation in two geoemydid turtles: Ocadia sinensis and Turtle Program, http://www.asianturtleprogram.org/pages/TCC/ Mauremys mutica. Aquaculture 305:138–142. Khanh_Hoa_turtle_transfer_16May13/2013-05-Khanh-Hoa- Duc, L.T. and Nguyen, T.L. 2001. Status of the Vietnamese Turtle Mauremys-transfer-16May13.pdf (Mauremys annamensis Siebenrock, 1903a) in the wild and in the Honda, M., Yasukawa, Y., Hirayama, R., and Ota, H. 2002a. trade in Quang Nam and Da Nang, preliminary report. Unpublished Phylogenetic relationships of the Asian box turtles of the genus Geoemydidae — Mauremys annamensis 081.13

Cuora sensu lato (Reptilia: Bataguridae) inferred from mitochondrial McCormack, T., Hoang, V.H., Hendrie, D., Nguyen, V.H., and Hudson, DNA sequences. Zoological Science 19(11):1305–1312. R. 2013. Development plan for Quang Ngai Turtle Assurance Honda, M., Yasukawa, Y., and Ota, H. 2002b. Phylogeny of the Colony (TAC) and Species Habitat Conservation Area (SHCA) for Eurasian freshwater turtles of the genus Mauremys Gray 1869 the Vietnamese Pond Turtle (Mauremys annamensis). Unpublished (Testudines), with special reference to a close affinity ofMauremys report of the Asian Turtle Program, 28 pp. japonica with Chinemys reevesii. Journal of Zoological Systematics McDowell, S.B. 1964. Partition of the genus Clemmys and related and Evolutionary Research 40(4):195–200. problems in the taxonomy of the aquatic Testudinidae. Proceedings Hu, Q., Huang, C., Xu, S., Zhang, Q., Ma, N., and Zhong, H. 2013. of the Zoological Society of London 143(2):239–279. [Primary phylogenies of Mauremys guangxiensis and Mauremys Nguyen, V.S., Ho, T.C., and Nguyen, Q.T. 2009. Herpetofauna of iversoni inferred from DNA sequences of mitochondrial ND4 gene Vietnam. Frankfurt am Main, Germany: Edition Chimaira, 768 pp. and nuclear c-mos gene] (in Chinese with English abstract). Sichuan Nguyen, X.V., Vu, N.L., Simpson, B.K., Ngo, V.T., Lai, T.Q., Huynh, X.Q., Journal of 32(2):180–186. and Vo, V.D. 2005. Status of the freshwater crocodile (Crocodylus International Species Information System. 2013. Zoological siamensis) in Song Hinh District, Phu Yen Province. Ho Chi Minh Information Management System. http://zims.isis.org. City, Vietnam: Institute of Tropical Biology and Fauna & Flora Ipser, T. 2011. Über Schildkröten und was einem sonst noch anhängt. International Programme, Technical Report, p. 50. Sacalia 9(31):6–56. Okada, Y., Yabe, T., and Oda, S.-I. 2010. Temperature-dependent IUCN. 2014. IUCN Red List of Threatened Species. Version 2014.1. sex determination in the , Mauremys japonica http://www.iucnredlist.org. (Reptilia: Geoemydidae). Current Herpetology 29(1):1–10. Iverson, J. 1992. A Revised Checklist with Distribution Maps of the Parham, J.F., Stuart, B.L., and Orlov, N.L. 2006. Geographic Turtles of the World. Richmond, IN: Privately published, 363 pp. distribution: Mauremys annamensis. Herpetological Review Iverson, J.B. and McCord, W.P. 1994. Variation in East Asian Turtles 37(2):239. of the genus Mauremys (Bataguridae; Testudines). Journal of Petzold, H.-G. 1963. Über einige Schildkröten aus Nord-Vietnam im Herpetology 28(2):178–187. Tierpark Berlin. Senckenbergiana Biologica. 44(1):1–-20. Jenkins, M.D. 1995. Tortoises and Freshwater Turtles: The Trade in Petzold, H.-G. 1965. Cuora galbinifrons und andere südostasiatische Southeast Asia. Cambridge, UK: TRAFFIC International, 48 pp. Schildkröten im Tierpark Berlin. Die Aquarien und Terrarien Kawata, K. 2003. Reptiles in Japanese collections. Part 1: chelonians, Zeitschrift 18(3/4):89–91,119–121. 1998. International Zoo News 50(5):265–275. Pham, T.T.H. 2012. Hybrid between Vietnamese Pond Turtle and Le, D.D. and Broad, S. 1995. Investigations into Tortoise and Chinese Stripe Necked Turtle found in central Vietnam. Press Freshwater Turtle Trade in Vietnam. Gland, Switzerland and release of the Asian Turtle Program. http://www.asianturtleprogram. Cambridge, UK: IUCN Species Survival Commission, 34 pp. org/pages/map_project/Hybrid_Mauremys_6Sep12/Hybrid_ Le, M., Hoang, T., and Le, D. 2004. Trade data and some comments Mauremys_1Jun12.htm on the distribution of Mauremys annamensis (Siebenrock, 1903). Qin, J.-Q. 1992 [1991]. A new species of genus Clemmys: C. Asiatic Herpetological Research 10:110–113. guangxiensis. In: Qian, Y.–M., Zhao, E.–M., and Zhao, K.–T. Lee, K.S., Lau, M.W.N., and Chan, B.P.L. 2004. Wild animal trade (Eds.). Animal Science Research. A volume issued to celebrate monitoring at selected markets in Guangzhou and Shenzhen, South the 90th birthday of Mangven L.–Y. Chang. China Forestry Press, China, 2000-2003. KFBG Technical Report Number 2. Hong Kong Beijing (12)2:60–62. SAR: Kadoorie Farm and Botanic Garden, 36 pp. Raffel, M. and Meier, E. 2013. Best year ever at the International Leviton, A.E. 1953. Catalogue of the amphibian and types in Centre for the Conservation of Turtles (IZS) at Muenster Zoo. the Natural History Museum of Stanford University. Herpetologica Turtle Survival, p. 10. 8(4):121–-132. Savage, J.M. 1953. Remarks on the Indo-chinese turtle Annamemys Li, G.-S., Fang, K., and Tang, T. 2002. [Techniques for rearing the merkleni; with special reference to the status of Cyclemys annamensis. turtle of Annamemys annamensis] (in Chinese). Reservoir Fisheries Annals and Magazine of Natural History 6(66):468–472. 22(3):19. Schecter, A., Birnbaum, L., Ryan, J.J., and Constable, J.D. 2006. López, D.M., Massana, J.S., and Silvestre, A.M. 2001. Annamemys Dioxins: an overview. Environmental Research 101(3):419–428. annamensis, Vietnamese turtle in grave danger of extinction. Shaffer, C. 2006. Vietnamese Pond Turtle program. Turtle and Tortoise Reptilia 18:13–15. Newsletter 9:13–14. McCord, W.P. and Iverson, J.B. 1994. A new species of Ocadia Shelby-Walker, J.A., Ward, C.K., and Mendonça, M.T. 2009. (Testudines: Batagurinae) from southwestern China. Proceedings Reproductive parameters in female yellow-blotched map turtles of the Biological Society of Washington 107(1):52–59. ( flavimaculata) from a historically contaminated site vs. McCormack, T. 2013. Research and conservation action for tortoises a reference site. Comparative Biochemistry and Physiology Part A: and freshwater turtles in Indo-Burma, final report. Unpublished Molecular and Integrative Physiology 154(3):401–408. report to the Critical Ecosystem Partnership Fund, 37 pp. Siebenrock, F. 1903. Schildkröten des östlichen Hinterindien. McCormack, T. and Bui, D.P. 2005. Clutch and incubation results Sitzungsberichte der Kaiserlichen Akademie der Wissenschaften of 2003 and 2004 for the Vietnamese Pond Turtle (Mauremys in Wien (Mathemathisch-Naturwissenschaftliche Klasse) annamensis) maintained in captivity at the Turtle Conservation 112(1):333–353. Centre (TCC), Cuc Phuong National Park, Vietnam. Unpublished Simpson, B.K. and Bezuijen, M. R. 2010. Siamese crocodile, Crocodylus report to the Asian Turtle Conservation Network, 4 pp. siamensis. In: Manolis, S.C. and Stevenson, C. (Eds.). Crocodiles. McCormack, T., Hendrie, D., and Nguyen, X.T. 2007. Rediscovery Status Survey and Conservation Action Plan. Third Edition. Darwin, after 67 years of the critically endangered Vietnamese Pond Turtle, Australia: Crocodile Specialist Group, pp. 120–126. Mauremys annamensis, in central Vietnam. In: Schaffer, C. (Ed.). Socialist Republic of Vietnam. 2006. [Decree 32/2006/ND-CP dated Program and Abstracts of the Fifth Annual Symposium on the 30th March 2006 on Management of Endangered, Precious, and Conservation and Biology of Tortoises and Freshwater Turtles. Rare Species of Wild Plants and Animals] (in Vietnamese). Atlanta, GA: Turtle Survival Alliance, p. 26. Socialist Republic of Vietnam. 2012. CITES CoP16 Prop 35 – Transfer 081.14 Conservation Biology of Freshwater Turtles and Tortoises • Chelonian Research Monographs, No. 5

of Mauremys annamensis from Appendix II to Appendix I. Geneva, Compilation Project of the IUCN/SSC Tortoise and Freshwa- Switzerland: CITES Secretariat, 10 pp. http://www.cites.org/eng/ ter Turtle Specialist Group. Chelonian Research Monographs cop/16/prop/E-CoP16-Prop-35.pdf. 5(7):000.329–479. Spinks, P.Q. and Shaffer, H.B. 2007. Conservation phylogenetics Turtle Conservation Coalition [Rhodin, A.G.J., Walde, A.D., Horne, of the Asian box turtles (Geoemydidae, Cuora): mitochondrial B.D., van Dijk, P.P., Blanck, T., and Hudson, R. (Eds.)]. 2011. introgression, numts, and inferences from multiple nuclear loci. Turtles in Trouble: The World’s 25+ Most Endangered Tortoises and Conservation Genetics 8(3):641–657. Freshwater Turtles – 2011. Lunenburg, MA: IUCN/SSC Tortoise Spinks, P.Q., Shaffer, H.B., Iverson, J.B., and McCord, W.P. 2004. and Freshwater Turtle Specialist Group, Turtle Conservation Fund, Phylogenetic hypotheses for the turtle family Geoemydidae. Turtle Survival Alliance, Turtle Conservancy, Chelonian Research Molecular Phylogenetics and Evolution 32(1):164–182. Foundation, Conservation International, Wildlife Conservation Stellman, J.M., Stellman, S.D., Christian, R., Weber, T., and Society, and San Diego Zoo Global, 54 pp. Tomasallo, C. 2003. The extent and patterns of usage of Agent Turtle Ecology and Conservation Project. 2002. Preliminary Orange and other herbicides in Vietnam. Nature 422(6933):681–687. summary report: Conservation and ecology of Mauremys Sterling, E.J., Hurley, M.M., and Le, D.M. 2006. Vietnam: A Natural annamensis. Unpublished report of the Turtle Ecology and History. New Haven, CT: Yale University Press, 423 pp. Conservation Project – Vietnam, 3 pp. Stern, A.G. 2014. Mauremys annamensis Vietnamese Leaf Turtle Uhrig, D. and Lee, D.S. 2006. Care and captive breeding of the North American Regional Studbook. First edition, current to 24 highly endangered Vietnam pond turtle, Mauremys annamensis August 2014. Miami, FL: Zoo Miami, 20 pp. (Siebenrock, 1903). Radiata 15(1):3–10. Stuart, B.L. 2004. The harvest and trade of reptiles at U Minh Thuong van Dijk, P.P., Stuart, B.L., and Rhodin, A.G.J. (Eds). 2000. Asian National Park, southern Viet Nam. TRAFFIC Bulletin 20(1):25–34. Turtle Trade. Chelonian Research Monographs 2. Lunenburg, MA: Stuart, B.L. and Parham, J.F. 2007. Recent hybrid origin of three rare Chelonian Research Foundation, 164 pp. Chinese turtles. Conservation Genetics 8(1):169–175. Wildlife Conservation Society. 2008. Commercial wildlife farms in Stuart, B.L., Timmins, R.J., Hendrie, D.B., Lieng, S., Chun, S., Hout, Vietnam: a problem or solution for conservation? Hanoi, Vietnam: P., Heng, K., Touch, S.T., Prak, L.H., Chul, T., Compton, J., and Wildlife Conservation Society, 46 pp. Holloway, R. 2000. Turtle trade in Indochina: Regional summary Wildlife Conservation Society – China Program and China Endangered (Cambodia, , and Vietnam). In: van Dijk, P.P., Stuart, B.L., Species of Wild Fauna and Flora Import and Export Administrative and Rhodin, A.G.J. (Eds). Asian Turtle Trade. Chelonian Research Office. 2000. Turtle Trade in Shanghai: report on market survey. Monographs 2. Lunenburg, MA: Chelonian Research Foundation, Shanghai, China: Wildlife Conservation Society, 23 pp. pp. 74–76. Yasukawa, Y., Ota, H., and Iverson, J.B. 1996. Geographic variation Thuy, H.T.T., Tobschall, H.J., and An, P.V. 2000. Distribution of and sexual size dimorphism in Mauremys mutica (Cantor, 1842) heavy metals in urban soils – a case study of Danang-Hoian Area (Reptilia: Bataguridae), with description of a new subspecies from (Vietnam). Environmental Geology 39(6):603–610. the southern Ryukyus, Japan. Zoological Science 13(2):303–317. Tiedemann, F. and Häupl, M. 1980. Typenkatalog der Herpetologischen Yasukawa, Y., Yabe, T., and Ota, H. 2008. Mauremys japonica Sammlung. Teil II. Reptilia. Kataloge der wissenschaftlichen (Temminck and Schlegel 1835) – Japanese pond turtle. In: Rhodin, Sammlungen 4, Vertebrata 2. Vienna, Austria: Naturhistorisches A.G.J., Pritchard, P.C.H., van Dijk, P.P., Saumure, R.A., Buhlmann, Museum Wien, 79 pp. K.A., and Iverson, J.B. (Eds.). Conservation Biology of Freshwater Tiedemann, F., Häupl, M., Grillitsch, H. 1994. Katalog der Typen der Turtles and Tortoises: A Compilation Project of the IUCN/SSC Herpetologischen Sammlung nach dem Stand vom 1. Jänner 1994. Tortoise and Freshwater Turtle Specialist Group. Chelonian Research Teil II: Reptilia. Kataloge der wissenschaftlichen Sammlungen 10, Monographs No. 5, pp. 003.1–003.6. Vertebrata 4. Vienna, Austria: Naturhistorisches Museum Wien, Yen, M.-C., Chen, T.-C., Hu, H.-L., Tzeng, R.-Y., Dinh, D.T., Nguyen, 102 pp. T.T.T., and Wong, C. J. 2011. Interannual variation of the fall Tien, D.V. 1957. [Zoological study in central Vietnam: Vien Linh rainfall in central Vietnam. Journal of the Meteorological Society region in Quang-Tri Province] (in Russian). Zoologicheskii Zhurnal of Japan 89A:259–270. 36(8):1209–1216. Zhou, T., Blanck, T., McCord, W.P., and Li, P.P. 2008. Tracking Cuora Tordoff, A.W., Tran, Q.B., Nguyen, D.T., and Le, M.H. (Eds.). 2004. mccordi Ernst, 1988: The first records of its natural habitat; a re- Sourcebook of existing and proposed protected areas in Vietnam, description; with data on captive populations and its vulnerability. second edition. Hanoi, Vietnam: BirdLife International in Indochina Hamadryad 32(1):57–69. and the Ministry of Agriculture and Rural Development. http:// birdlifeindochina.org/birdlife/source_book/index.html. Citation Format for this Account: Tran, K., Ho, C.T., Nguyen, S.V., and Pham, T. 2007. [Reptiles and amphibians] (in Vietnamese). In: Dang, N.T., Tran, K., Dang, H.H., McCormack, T.E.M., Dawson, J.E., Hendrie, D.B., Ewert, M.A., Nguyen, C., Nguyen, T.N., Nguyen, Y.N. and Dang, D.T. (Eds.). Iverson, J.B., Hatcher, R.E., and Goode, J.M. 2014. Mauremys [Vietnam Red Data Book. Part 1. Animals]. Hanoi, Vietnam: Science annamensis (Siebenrock 1903) – Vietnamese Pond Turtle, Annam and Technics Publishing House, pp. 219–276. Pond Turtle, Rùa Trung Bộ. In: Rhodin, A.G.J., Pritchard, P.C.H., TTWG – Turtle Taxonomy Working Group [van Dijk, P.P., Iver- van Dijk, P.P., Saumure, R.A., Buhlmann, K.A., Iverson, J.B., and son, J.B., Rhodin, A.G.J., Shaffer, H.B., and Bour, R.]. 2014. Mittermeier, R.A. (Eds.). Conservation Biology of Freshwater Turtles of the world, 7th edition: annotated checklist of taxonomy, Turtles and Tortoises: A Compilation Project of the IUCN/SSC synonymy, distribution with maps, and . In: Tortoise and Freshwater Turtle Specialist Group. Chelonian Rhodin, A.G.J., Pritchard, P.C.H., van Dijk, P.P., Saumure, R.A., Research Monographs 5(7):081.1–14, doi:10.3854/crm.5.081. Buhlmann, K.A., Iverson, J.B., and Mittermeier, R.A. (Eds.). annamensis.v1.2014, http://www.iucn-tftsg.org/cbftt/. Conservation Biology of Freshwater Turtles and Tortoises: A